Ixodes persulcatus/pavlovskyi natural hybrids in Siberia: Occurrence in sympatric areas and infection by a wide range of tick-transmitted agents

Рар, В. А.; Ливанова, Н. Н.; Sabitova, Yuliya; Igolkina, Yana; Tkachev, Sergey; Tikunov, Artem; Бабкин, И. В.; Golovljova, Irina; Panov, Victor V.; Tikunova, Nina

doi:10.1016/j.ttbdis.2019.05.020

Cited by 11 publications

(17 citation statements)

References 33 publications

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“…Subsequently it was discovered to be occurring sympatrically with B. burgdorferi sensu lato in several Ixodes species that also transmit Lyme disease spirochetes. These included Ixodes persulcatus in Eurasia [2][3][4][5][6][7], I. scapularis [8][9][10][11] and I. pacificus [12][13][14][15] in North America, and I. ricinus in Europe [16][17][18][19][20]. The prevalence of B. miyamotoi in ticks was found to be usually lower than that of B. burgdorferi s.l.…”

Section: Introductionmentioning

confidence: 99%

Whole genome sequencing of Borrelia miyamotoi isolate Izh-4: reference for a complex bacterial genome

Kuleshov

Margos²,

Fingerle³

et al. 2020

BMC Genomics

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Background: The genus Borrelia comprises spirochaetal bacteria maintained in natural transmission cycles by tick vectors and vertebrate reservoir hosts. The main groups are represented by a species complex including the causative agents of Lyme borreliosis and relapsing fever group Borrelia. Borrelia miyamotoi belongs to the relapsing fever group of spirochetes and forms distinct populations in North America, Asia, and Europe. As all Borrelia species B. miyamotoi possess an unusual and complex genome consisting of a linear chromosome and a number of linear and circular plasmids. The species is considered an emerging human pathogen and an increasing number of human cases are being described in the Northern hemisphere. The aim of this study was to produce a high quality reference genome that will facilitate future studies into genetic differences between different populations and the genome plasticity of B. miyamotoi. Results: We used multiple available sequencing methods, including Pacific Bioscience single-molecule real-time technology (SMRT) and Oxford Nanopore technology (ONT) supplemented with highly accurate Illumina sequences, to explore the suitability for whole genome assembly of the Russian B. miyamotoi isolate, Izh-4. Plasmids were typed according to their potential plasmid partitioning genes (PF32, 49, 50, 57/62). Comparing and combining results of both long-read (SMRT and ONT) and short-read methods (Illumina), we determined that the genome of the isolate Izh-4 consisted of one linear chromosome, 12 linear and two circular plasmids. Whilst the majority of plasmids had corresponding contigs in the Asian B. miyamotoi isolate FR64b, there were only four that matched plasmids of the North American isolate CT13-2396, indicating differences between B. miyamotoi populations. Several plasmids, e.g. lp41, lp29, lp23, and lp24, were found to carry variable major proteins. Amongst those were variable large proteins (Vlp) subtype Vlp-α, Vlp-γ, Vlp-δ and also Vlp-β. Phylogenetic analysis of common plasmids types showed the uniqueness in Russian/Asian isolates of B. miyamotoi compared to other isolates. Conclusions: We here describe the genome of a Russian B. miyamotoi clinical isolate, providing a solid basis for future comparative genomics of B. miyamotoi isolates. This will be a great impetus for further basic, molecular and epidemiological research on this emerging tick-borne pathogen.

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Section: Introductionmentioning

confidence: 99%

Whole genome sequencing of Borrelia miyamotoi isolate Izh-4: reference for a complex bacterial genome

Kuleshov

Margos²,

Fingerle³

et al. 2020

BMC Genomics

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“…Ixodes persulcatus, a tick species distributed widely from the eastern Baltic coast to Japan (22)(23)(24)(25), has been reported to harbour symbionts including the Montezuma agent, now called Candidatus Lariskella arthropodarum (26)(27)(28), Coxiella and Spiroplasma spp. (29), as well as human and livestock pathogens including tick-borne encephalitis virus (TBEV), Kemerovo virus, Alongshan virus, Anaplasma phagocytophilum, Candidatus Neoehrlichia mikurensis, Ehrlichia muris, Rickettsia helvetica, Rickettsia heilongjiangensis, Candidatus Rickettsia tarasevichiae, Borrelia miyamotoi, Borrelia burgdorferi sensu lato, Theileria equi and several species of Babesia (25,(30)(31)(32)(33)(34)(35)(36)(37)(38). Co-infections with multiple pathogens and symbionts are common (29,35,39).…”

Section: Introductionmentioning

confidence: 99%

Spiroplasma Isolated From Third-Generation Laboratory Colony Ixodes persulcatus Ticks

et al. 2021

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Spiroplasma are vertically-transmitted endosymbionts of ticks and other arthropods. Field-collected Ixodes persulcatus have been reported to harbour Spiroplasma, but nothing is known about their persistence during laboratory colonisation of this tick species. We successfully isolated Spiroplasma from internal organs of 6/10 unfed adult ticks, belonging to the third generation of an I. persulcatus laboratory colony, into tick cell culture. We screened a further 51 adult male and female ticks from the same colony for presence of Spiroplasma by genus-specific PCR amplification of fragments of the 16S rRNA and rpoB genes; 100% of these ticks were infected and the 16S rRNA sequence showed 99.8% similarity to that of a previously-published Spiroplasma isolated from field-collected I. persulcatus. Our study shows that Spiroplasma endosymbionts persist at high prevalence in colonised I. persulcatus through at least three generations, and confirms the usefulness of tick cell lines for isolation and cultivation of this bacterium.

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“…The causative agents of North Asian tick-borne spotted fever, R. sibirica and Rickettsia heilongjiangensis , are also well recognized human pathogens that are usually associated with Dermacentor nuttalli (Olenev, 1928) and Haemaphysalis concinna (Koch, 1884) ticks, respectively [ 13 , 14 ]. However, the infection of I. persulcatus with R. sibirica and R. heilongjiangensis has also been described [ 15 ]. In Mongolia, around 4% of Dermacentor sp.…”

Section: Introductionmentioning

confidence: 99%

“…simultaneous infection of the same tick specimen with two or more microorganisms. For I. persulcatus , co-infections with multiple pathogens have been studied in different parts of the distribution range, including Japan [ 17 – 19 ], Russia [ 15 , 20 – 22 ] and Finland [ 23 ]. It has been shown that in different geographic locations co-infecting microorganisms can either have no effect on each other, such as TBEV, B. burgdorferi s.l.…”

Section: Introductionmentioning

confidence: 99%

Co-infections with multiple pathogens in natural populations of Ixodes persulcatus ticks in Mongolia

et al. 2022

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Background In Mongolia, the taiga tick Ixodes persulcatus is the major vector of tick-borne pathogens. Knowledge about co-infections of these pathogens in ticks is necessary both for understanding their persistence in nature and for diagnosing and treating tick-borne diseases. Methods The prevalence of seven tick-borne infections in 346 I. persulcatus collected from the Selenge and Bulgan provinces of Mongolia was evaluated using real-time PCR. Quantification of Borrelia spp. was performed using multiplex quantitative PCR targeting the 16S rRNA gene. Genetic analysis of Borrelia spp. in 11 ticks infected with Borrelia miyamotoi, including six ticks co-infected with Borrelia burgdorferi sensu lato (s.l.), was performed by high-throughput sequencing of the flaB gene fragment. Results Six ticks (1.7%) were infected with tick-borne encephalitis virus (TBEV); 171 (49.4%), with B. burgdorferi sensu lato; 17 (4.9%), with B. miyamotoi; 47 (13.6%), with Anaplasma phagocytophilum; and 56 (16.2%), with Ehrlichia sp. Neither Rickettsia sibirica nor R. heilongjiangensis were detected. Borrelia burgdorferi s.l. occurred as co-infection in 55 (32.2%) of all infected ticks. The other pathogens co-infected ticks in 58.8–70.2% of cases. No pairwise associations between co-infecting pathogens were observed, with the exception of a positive association between A. phagocytophilum and Ehrlichia sp. infections. The spirochete loads of B. miyamotoi were significantly higher than those of B. burgdorferi s.l. (mean: 5.2 vs 4.0 log10 genome copies/tick, respectively). Ten isolates of B. miyamotoi belonged to the Siberian lineage. Borrelia burgdorferi s.l was represented by nine isolates of B. afzelii, B. bavariensis and B. garinii. Conclusions In populations of I. persulcatus inhabiting the Selenge and Bulgan provinces of Mongolia, five vector-borne pathogens, i.e. TBEV, B. burgdorferi s.l., B. miyamotoi, A. phagocytophilum and Ehrlichia sp., persist independently from each other, with the exception of A. phagocytophilum and Ehrlichia sp. which seem to share the circulation mode. The discrepancies in B. burgdorferi s.l. and B. miyamotoi prevalence and spirochete load per tick suggest that different ecological niches are occupied by Lyme disease and relapsing fever agents. High-throughput sequencing allows genetic identification of borreliae species in co-infected ticks. Graphical Abstract

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Ixodes persulcatus/pavlovskyi natural hybrids in Siberia: Occurrence in sympatric areas and infection by a wide range of tick-transmitted agents

Cited by 11 publications

References 33 publications

Whole genome sequencing of Borrelia miyamotoi isolate Izh-4: reference for a complex bacterial genome

Whole genome sequencing of Borrelia miyamotoi isolate Izh-4: reference for a complex bacterial genome

Spiroplasma Isolated From Third-Generation Laboratory Colony Ixodes persulcatus Ticks

Co-infections with multiple pathogens in natural populations of Ixodes persulcatus ticks in Mongolia

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